Common Neocortical and Hippocampal Correlates of Performance Errors in a Timing Task

We aimed to identify the neuronal correlates of performance errors in a difficult timing task. Male rats were trained to seek rewards and avoid shocks depending on the position of photic conditioned stimuli (CS-R and CS-S, respectively). Then, they were exposed to conflict trials where they had to time the interval between the CS-R and CS-S to obtain rewards while avoiding footshocks. There were pronounced individual differences in behavioral strategies on conflict trials. When presented with a CS-S, some rats quickly left the shock sector, forsaking the option of earning a reward, and rarely got shocked. Others earned rewards by delaying avoidance based on the interval between the CS-R and CS-S but were shocked more often. The probability rats would fail a given trial was not stable across trials as rats engaged in incorrect trial runs that were longer than expected by chance. Since this finding suggested that rats shift between two quasi-stable processing modes, we next examined the neuronal correlates of errors. Incorrect trials coincided with reduced firing rates in CA1 and sensory cortical neurons. Moreover, trial-to-trial variations in the firing rates of simultaneously recorded neurons were more strongly correlated on error than correct trials. Last, the power of low-frequency local field potential oscillations was higher during incorrect trials. The finding that the neuronal correlates of correct and error trials are similar in the hippocampus and neocortex lead us to hypothesize that they depend on changes in the activity of common afferents, such as neuromodulatory inputs.